Latent gene network expression underlies the reversion of a polyphenic trait in the worker caste of ants

Polyphenism, in which alternative phenotypes develop from the same genome in response to environmental cues, is widespread in nature. Yet, the developmental processes that facilitate evolution of polyphenic traits remain poorly understood. We address this question in ants, where caste polyphenism is key to their division of labor, producing winged reproductive castes (queens and males) and a wingless non-reproductive worker caste. Here, we investigate the expression of a gene regulatory network (GRN) underlying the evolution and development of a caste-specific trait in ants–the ocelli–3 simple single-lens eyes on the dorsal head of flying insects. We focus on a hyperdiverse subfamily of ants (Formicinae), where 3 ocelli are always present in males and queens, while the worker caste shows dramatic variation in the presence / absence or number of ocelli across species. We discovered that ocelli in the worker caste underwent at least 3 independent and partial phylogenetic reversions, giving rise to workers with only a single ocellus. We also discovered that, in two closely related species whose adult workers completely lack ocelli, the ocelli GRN remains expressed throughout larval head development and is interrupted only in downstream genes at later stages. Consequently, rudimentary ocelli transiently appear in pupae but disappear before adulthood. This latent expression of the ocelli GRN therefore facilitated these partial reversions to a single ocellus, leading to a novel phenotypic pattern of ocelli in the worker caste. We propose that latent developmental potentials may generally underlie polyphenic traits and facilitate full or partial reversion with novel phenotypic patterns.